Biochemical characterization of potential virulence markers in the human fungal pathogen Pseudallescheria boydii

References

• Kwon-Chung KJ, Bennett JE. Pseudallescheriasis and Scedosporium. Medical Mycology, KJ Kwon-Chung, JE Bennett. Lea and Febiger, Philadelphia 1992; 678–694
   Google Scholar
• De Hoog, GS, Guarro, J, Gene, J, Figueras, MJ. Atlas of Clinical Fungi, 2nd. edn. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands, and University Rovira i Virgili, Reus, Spain, 2000
   Google Scholar
• Steinbach WJ, Perfect JR. Scedosporium species infections and treatments. J Chemother 2003; 15: 16–27
   PubMed Web of Science ®Google Scholar
• Defontaine A, Zouhair R, Cimon B, et al. Genotyping study of Scedosporium apiospermum isolates from patients with cystic fibrosis. J Clin Microbiol 2002; 40: 2108–2114
   PubMed Web of Science ®Google Scholar
• Guarro J, Kantarcioglu AS, Horre R, et al. Scedosporium apiospermum: changing clinical spectrum of a therapy-refractory opportunist. Med Mycol 2006; 44: 295–327
   PubMed Web of Science ®Google Scholar
• Lopez FA, Crowley RS, Wastila L, Valantine HA, Remington JS. Scedosporium apiospermum (Pseudallescheria boydii) infection in a heart transplant recipient: a case of mistaken identity. J Heart Lung Transpl 1998; 17: 321–324
   PubMed Web of Science ®Google Scholar
• Kleinschmidt-de-Masters BK. Central nervous system aspergillosis: a 20-year retrospective series. Hum Pathol 2002; 33: 116–124
   Google Scholar
• Gueho E, De Hoog GS. Taxonomy of the medical species of Pseudallescheria and Scedosporium. J Mycol Med 1991; 1: 3–9
   Google Scholar
• Rainer J, De Hoog GS, Wedde M, Graser I, Gilges S. Molecular variability of Pseudallescheria boydii, a neurotropic opportunist. J Clin Microbiol 2000; 38: 3267–3273
   PubMed Web of Science ®Google Scholar
• Zeng JS, Fukushima K, Takizawa K, et al. Intraspecific diversity of species of the Pseudallescheria boydii complex. Med Mycol 2007; 45: 547–558
   PubMed Web of Science ®Google Scholar
• Gordon MA. Nutrition and sporulation of Allescheria boydii. J Bacteriol 1957; 73: 199–205
   Google Scholar
• Cazin J, Decker DW. Carbohydrate nutrition and sporulation of Allescheria boydii. J Bacteriol 1964; 88: 1624–1628
   Google Scholar
• Cazin J, Decker DW. Growth of Allescheria boydii in antibiotic-containing media. J Bacteriol 1965; 90: 1308–1313
   Google Scholar
• Carrillo A, Guarro J. In vitro activities of four novel triazoles against Scedosporium spp. Antimicrob Agents Chemother 2001; 45: 2151–2153
   PubMed Web of Science ®Google Scholar
• Capilla J, Serena C, Pastor FJ, Ortoneda M, Guarro J. Efficacy of voriconazole in treatment of systemic scedosporiosis in neutropenic mice. Antimicrob Agents Chemother 2004; 48: 4009–4011
   PubMedGoogle Scholar
• Gilgado F, Cano J, Gene J, Guarro J. Molecular phylogeny of the Pseudallescheria boydii species complex: proposal of two new species. J Clin Microbiol 2005; 43: 4930–4942
   PubMed Web of Science ®Google Scholar
• Gil-Lamaignere C, Maloukou A, Rodriguez-Tudela JL, Roilides E. Human phagocytic cell responses to Scedosporium prolificans. Med Mycol 2001; 39: 169–175
   PubMed Web of Science ®Google Scholar
• Gil-Lamaignere C, Roilides E, Lyman CA, et al. Human phagocyte cell responses to Scedosporium apiospermum (Pseudallescheria boydii): variable susceptibility to oxidative injury. Infect Immun 2003; 71: 6472–6478
   PubMed Web of Science ®Google Scholar
• Bittencourt VCB, Figueiredo RT, da Silva RB, et al. An alpha-glucan of Pseudallescheria boydii is involved in fungal phagocytosis and Toll-like receptor activation. J Biol Chem 2006; 281: 22614–22623
   PubMed Web of Science ®Google Scholar
• E Barreto-Bergter, Pinto, MR, Rodrigues, ML, Bittencourt, VBC, Gorin, PAJ.. Hugo Verli. Structural and functional aspects of fungal polysaccharides, peptidopolysaccharides and ceramide monohexosides. In:. Insights into Carbohydrate Structure and Biological Function. 2006; 147–173. Transworld Research Network: KeralaIndia.
   Google Scholar
• Pinto MR, Mulloy B, Haido RM, Travassos LR, Barreto-Bergter E. A peptidorhamnomannan from the mycelium of Pseudallescheria boydii is a potential diagnostic antigen of this emerging human pathogen. Microbiology 2001; 147: 1499–1506
   PubMed Web of Science ®Google Scholar
• Lopes-Alves L, Travassos LR, Previato JO, Mendonça-Previato L. Novel antigenic determinants from peptidorhamnomannans of Sporothrix schenckii. Glycobiology 1994; 4: 281–288
   Google Scholar
• Pinto MR, Gorin PA, Wait R, Mulloy B, Barreto-Bergter E. Structures of the O-linked oligosaccharides of a complex glycoconjugate from Pseudallescheria boydii. Glycobiology 2005; 15: 895–904
   PubMedGoogle Scholar
• Leitão EA, Bittencourt VC, Haido RM, et al. Beta-galactofuranose-containing O-linked oligosaccharides present in the cell wall peptidogalactomannan of Aspergillus fumigatus contain immunodominant epitopes. Glycobiology 2003; 13: 681–692
   PubMed Web of Science ®Google Scholar
• Penha CV, Bezerra LM. Concanavalin A-binding cell wall antigens of Sporothrix schenckii: a serological study. Med Mycol 2000; 38: 1–7
   PubMed Web of Science ®Google Scholar
• Pinto MR, de Sá AC, Limongi CL, et al. Involvement of peptidorhamnomannan in the interaction of Pseudallescheria boydii and HEp2 cells. Microbes Infect 2004; 6: 1259–1267
   PubMed Web of Science ®Google Scholar
• Osherov N, May GS. The molecular mechanisms of conidial germination. FEMS Microbiol Lett 2001; 199: 153–160
   PubMed Web of Science ®Google Scholar
• Barreto-Bergter E, Pinto MR, Rodrigues ML. Structure and biological functions of fungal cerebrosides. An Acad Bras Ciênc 2004; 76: 67–84
   PubMed Web of Science ®Google Scholar
• Saito K, Takakuwa N, Ohnishi M, Oda Y. Presence of glucosylceramide in yeast and its relation to alkali tolerance of yeast. Appl Microbiol Biotechnol 2006; 71: 515–521
   Google Scholar
• Rodrigues ML, Travassos LR, Miranda KR, et al. Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infect Immun 2000; 8: 7049–7060
   Google Scholar
• Rodrigues ML, Shi L, Barreto-Bergter E, et al. A monoclonal antibody to fungal glucosylceramide protects mice against lethal Cryptococcus neoformans infection. Clin Vaccine Immunol 2007; 14: 1372–1376
   PubMedGoogle Scholar
• Toledo MS, Levery SB, Suzuki E, Straus AH, Takahashi HK. Characterization of cerebrosides from the thermally dimorphic mycopathogen Histoplasma capsulatum expression of 2-hydroxy fatty N-acyl(E)-Δ3-unsaturation correlates with the yeast-mycelium phase transition. Glycobiology 2001; 11: 113–124
   Google Scholar
• Levery SB, Momany M, Lindsey R, et al. Disruption of the glucosylceramide biosynthetic pathway in Aspergillus nidulans and Aspergillus fumigatus by inhibitors of UDP-Glc:ceramide glucosyltransferase strongly affects spore germination, cell cycle, and hyphal growth. FEBS Lett 2002; 525: 59–64
   PubMed Web of Science ®Google Scholar
• Pinto MR, Rodrigues ML, Travassos LR, et al. Characterization of glucosylceramides in Pseudallescheria boydii and their involvement in fungal differentiation. Glycobiology 2002; 12: 251–260
   PubMed Web of Science ®Google Scholar
• Silva AF, Rodrigues ML, Farias SE, et al. Glucosylceramides in Colletotrichum gloeosporioides are involved in the differentiation of conidia into mycelial cells. FEBS Lett 2004; 561: 137–143
   Google Scholar
• Nimrichter L, Cerqueira MD, Leitão EA, et al. Structure, cellular distribution, antigenicity, and biological functions of Fonsecaea pedrosoi ceramide monohexosides. Infect Immun 2005; 73: 7860–7868
   PubMedGoogle Scholar
• Ritterhaus PC, Kechichian TB, Allegood JC, et al. Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest 2006; 116: 1651–1659
   Google Scholar
• Thevissen K, Warnecke DC, Francois IE, et al. Defensins from insects and plants interact with fungal glucosylceramides. J Biol Chem 2004; 279: 3900–3905
   PubMed Web of Science ®Google Scholar
• Aerts AM, Francois IE, Meert EM, et al. The antifungal activity of RsAFP2, a plant defensin from Raphanus sativus, involves the induction of reactive oxygen species in Candida albicans. J Mol Microbiol Biotechnol 2007; 13: 243–247
   PubMed Web of Science ®Google Scholar
• Dickson RCC, Sumanasekera C, Lester RL. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 2006; 45: 447–465
   PubMed Web of Science ®Google Scholar
• Luberto C, Toffaletti DL, Wills EA, et al. Roles for inositol-phosphoryl ceramide synthase 1 (IPC1) in pathogenesis of Cryptococcus neoformans. Gene Dev 2001; 15: 201–212
   PubMed Web of Science ®Google Scholar
• Leipelt M, Warnecke D, Zahringer U, et al. Glucosylceramide synthases, a gene family responsible for the biosynthesis of glycosphingolipids in animals, plants, and fungi. J Biol Chem 2001; 276: 33621–33629
   PubMedGoogle Scholar
• Bahia MCFS, Haido RMT, Figueiredo MHG, et al. Humoral immune response in aspergillosis: an immunodominant glycoprotein of 35 kDa from Aspergillus flavus. Curr Microbiol 2003; 47: 163–168
   Google Scholar
• Dinadayala P, Lemassu A, Granovski P, et al. Revisiting the structure of the anti-neoplastic glucans of Mycobacterium bovis Bacille Calmette-Guerin. Structural analysis of the extracellular and boiling water extract-derived glucans of the vaccine substrains. J Biol Chem 2004; 279: 12369–12378
   PubMed Web of Science ®Google Scholar
• Zang LH, Howseman AM, Shulman RG. Assignment of the 1H chemical shifts of glycogen. Carbohydr Res 1991; 220: 1–9
   Web of Science ®Google Scholar
• Carpenter S, O'Neill LA. How important are Toll-like receptors for antimicrobial responses?. Cell Microbiol 2007; 9: 1891–1901
   PubMed Web of Science ®Google Scholar
• Miyazaki T, Kohno S, Mitsutake K, et al. Plasma (1→3)-β-d-glucan and fungal antigenemia in patients with candidemia, aspergillosis, and cryptococcosis. J Clin Microbiol 1995; 33: 3115–3118
   PubMed Web of Science ®Google Scholar
• Kedzierska A, Kochan P, Pietrzyk A, Kedzierska J. Current status of fungal cell wall components in the immunodiagnostics of invasive fungal infections in humans: galactomannan, mannan and (1→3)-β-d-glucan antigens. Eur J Clin Microbiol Infect Dis 2007; 26: 755–766
   PubMed Web of Science ®Google Scholar
• Hohl TM, van Epps HL, Rivera A, et al. Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 2005; 1: e30
   PubMed Web of Science ®Google Scholar
• Brown GD, Herre J, Williams DL, et al. Dectin-1 mediates the biological effects of beta-glucans. J Exp Med 2003; 197: 1119–1124
   PubMed Web of Science ®Google Scholar
• Reese AJ, Yoneda A, Breger JA, et al. Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol 2007; 63: 1385–1398
   PubMed Web of Science ®Google Scholar
• Borges-Walmsley MI, Chen D, Shu X, Walmsley AR. The pathobiology of Paracoccidioides brasiliensis. Trends Microbiol 2002; 10: 80–87
   PubMed Web of Science ®Google Scholar
• Rappleye CA, Engle JT, Goldman WE. RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 2004; 53: 153–165
   PubMed Web of Science ®Google Scholar
• Bellocchio S, Montagnoli C, Bozza S, et al. The contribution of Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 2004; 172: 3059–3069
   PubMed Web of Science ®Google Scholar
• Douglas CM. Fungal β(1→3)-d-glucan synthesis. Med Mycol 2001; 39(Suppl. 1)55–66
   PubMed Web of Science ®Google Scholar
• Pazos C, Ponton J, Palácio AD. Contribution of (1→3)-β-d-glucan chromogenic assay to diagnosis and therapeutic monitoring of invasive aspergillosis in neutropenic adult patients: a comparison with serial screening for circulating galactomannan. J Clin Microbiol 2005; 43: 299–305
   PubMed Web of Science ®Google Scholar
• Odabasi Z, Paetznick VL, Rodriguez JR, et al. Differences in beta-glucan levels in culture supernatants of a variety of fungi. Med Mycol 2006; 44: 267–72
   PubMed Web of Science ®Google Scholar
• Kahn JN, Hsu MJ, Racine F, Giacobbe R, Motyl M. Caspofungin susceptibility in Aspergillus and non-Aspergillus molds: inhibition of glucan synthase and reduction of beta-d-1,3 glucan levels in culture. Antimicrob Agents Chemother 2006; 50: 2214–2216
   PubMed Web of Science ®Google Scholar
• Canuto MM, Rodero FG. Antifungal drug resistance to azoles and polyenes. Lancet Infect Dis 2002; 2: 550–563
   PubMed Web of Science ®Google Scholar
• Pitson SM, Seviour RJ, McDougall BM. Noncellulolytic fungal β-glucanases: their physiology and regulation. Enz Microb Technol 1993; 15: 178–190
   PubMed Web of Science ®Google Scholar
• Hube B. Extracellular peptidases of human pathogenic fungi. Contrib Microbiol 2000; 5: 126–137
   Google Scholar
• Monod M, Capoccia S, Lechenne B, et al. Secreted proteases from pathogenic fungi. Int J Med Microbiol 2002; 292: 405–419
   PubMed Web of Science ®Google Scholar
• Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl peptidases in virulence and pathogenesis. Microbiol Mol Biol Rev 2003; 67: 400–428
   PubMed Web of Science ®Google Scholar
• Larcher G, Cimon B, Symoens F, et al. A 33 kDa serine proteinase from Scedosporium apiospermum. Biochem J 1996; 315: 119–126
   PubMed Web of Science ®Google Scholar
• Larcher G, Bouchara JP, Annaix V, et al. Purification and characterization of a fibrinogenolytic serine proteinase from Aspergillus fumigatus culture filtrate. FEBS Lett 1992; 308: 65–69
   PubMed Web of Science ®Google Scholar
• Silva BA, Santos ALS, Barreto-Bergter E, Pinto MR. Extracellular peptidase in the fungal pathogen Pseudallescheria boydii. Curr Microbiol 2006; 53: 18–22
   PubMed Web of Science ®Google Scholar
• Silva BA, Pinto MR, Soares RMA, Barreto-Bergter E, Santos ALS. Pseudallescheria boydii releases metallopeptidases capable of cleaving several proteinaceous compounds. Res Microbiol 2006; 157: 425–432
   Google Scholar
• Pereira MM, Silva BA, Pinto MR, Barreto-Bergter E, Santos ALS. Proteins and peptidases from conidia and mycelia of Scedosporium apiospermum strain HLPB. Mycopathologia 2009; 167: 25–30
   Google Scholar
• Cohen PTW. The structure and regulation of protein phosphatases. Annu Rev Biochem 1989; 58: 453–508
   PubMed Web of Science ®Google Scholar
• Zhan XL, Hong Y, Zhu T, et al. Essential functions of protein tyrosine phosphatase Ptp2 and Ptp3 and Rim 11 tyrosine phosphorylation in Sascharomyces cerevisiae meiosis and sporulation. Mol Biol Cell 2000; 11: 663–676
   PubMedGoogle Scholar
• Kiffer-Moreira T, Pinheiro AA, Pinto MR, et al. Mycelial forms of Pseudallescheria boydii present ectophosphatase activities. Arch Microbiol 2007; 188: 159–166
   PubMed Web of Science ®Google Scholar
• Fernanado PHP, Panagoda GJ, Samaranayare LP. The relation between the acid and alkaline phosphatase activity and the adherence of clinical isolates of Candida parapsilosis to human epithelial cell. APMIS 1999; 107: 1034–1042
   Google Scholar
• Belanger PH, Johnston DA, Fratti RA, Zhang M, Filler SG. Endocytosis of Candida albicans by vascular endothelial cells is associated with tyrosine phosphorylation of specific host cells proteins. Cell Microbiol 2002; 4: 805–812
   Google Scholar
• Nakagura KH, Tachibana H, Kaneda Y. Alteration of the cell surface acid phosphatase concomitant with morphological transformation in Trypanosoma cruzi. Comp Biochem Physiol 1985; 81: 815–817
   Google Scholar
• Bakalara N, Santarelli X, Davis C, Baltz T. Purification, cloning and characterization of an acid ectoprotein phosphatase differentially expressed in the infectious bloodstream form of Trypanosoma brucei. J Biol Chem 2000; 275: 8863–8871
   PubMedGoogle Scholar
• Touati E, Dassa E, Dassa J, Boquet PL. Acid phosphatase (pH2.5) of Escherichia coli: regulatory characteristics. Microorganisms, A Torriani-Gorini, FG Rothman, S Silver, A Wright, E Yagil. ASM Press, Washington, DC 1987; 31–40
   Google Scholar
• Hamilton AJ, Holdom MD. Antioxidant systems in the pathogenic fungi of man and their role in virulence. Med Mycol 1999; 37: 375–389
   PubMed Web of Science ®Google Scholar
• Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem 1995; 64: 97–112
   PubMed Web of Science ®Google Scholar
• Hamilton AJ, Holdom MD, Jeavons L. Expression of the Cu,Zn-superoxide dismutase of Aspergillus fumigatus as determined by immunohistochemistry and immunoelectron microscopy. FEMS Immunol Med Microbiol 1996; 14: 95–102
   Google Scholar
• Holdom MD, Hay RJ, Hamilton AJ. The Cu,Zn-superoxide dismutases of Aspergillus flavus, Aspergillus niger, Aspergillus nidulans and Aspergillus terreus: purification and biochemical comparison with the Aspergillus fumigatus Cu,Zn-superoxide dismutase. Infect Immun 1996; 64: 3326–3332
   PubMedGoogle Scholar
• Hwang CS, Rhie GE, Oh JH, et al. Copper- and zinc-containing superoxide dismutase (Cu/Zn-SOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 2002; 148: 3705–3713
   PubMed Web of Science ®Google Scholar
• Tesfa-Selase F, Hay RJ. Superoxide dismutase of Cryptococcus neoformans: purification and characterization. J Med Vet Mycol 1995; 33: 253–259
   Google Scholar
• Ungpakorn R, Holdom MD, Hamilton AJ, Hay RJ. Purification and partial characterization of the Cu,Zn-superoxide dismutase from the dermatophyte Trichophyton mentagrophytes var. interdigitale. Clin Exp Dermatol 1996; 21: 190–196
   PubMedGoogle Scholar
• Lima OC, Larcher G, Vandeputte P, et al. Molecular cloning and biochemical characterization of a Cu,Zn-superoxide dismutase from Scedosporium apiospermum. Microbes Infect 2007; 9: 558–565
   PubMed Web of Science ®Google Scholar
• Oberegger H, Zadra I, Schoeser M, Haas H. Iron starvation leads to increased expression of Cu/Zn-superoxide dismutase in Aspergillus. FEBS Lett 2000; 485: 113–116
   PubMedGoogle Scholar
• Haas H, Zada I, Stöffler G, Angermayr K. The Aspergillus nidulans GATA factor SREA is involved in regulation of siderophore biosynthesis and control of iron uptake. J Biol Chem 1999; 8: 4613–4619
   Google Scholar
• Kasahara K, Sanai Y. Possible roles of glycosphingolipids in lipid rafts. Biophys Chem 1999; 82: 121–127
   Google Scholar